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The Chromosomal Polymorphism of Drosophila Subobscura: a Microevolutionary Weapon to Monitor Global Change

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The Chromosomal Polymorphism of Drosophila Subobscura: a Microevolutionary Weapon to Monitor Global Change Heredity (2009) 103, 364–367 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy REVIEW The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change J Balanya`1, RB Huey2, GW Gilchrist3 and L Serra1 1Grup de Biologia Evolutiva, Departament de Gene`tica, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalonia, Spain; 2Department of Biology, University of Washington, Seattle, WA, USA and 3Department of Biology, College of William & Mary, Williamsburg, VA, USA The Palaearctic species Drosophila subobscura recently composition of populations. Indeed, the long-term variation of invaded the west coast of Chile and North America. This this polymorphism shows a general increase in the frequency of invasion helped to corroborate the adaptive value of the rich those inversions typical of low latitudes, with a corresponding chromosomal polymorphism of the species, as the same clinal decrease of those typical of populations closer to the poles. patterns than those observed in the original Palaearctic area Although the mechanisms underlying these changes are not were reproduced in the colonized areas in a relatively short well understood, the system remains a valid tool to monitor the period of time. The rapid response of this polymorphism to genetic impact of global warming on natural populations. environmental conditions makes it a good candidate to measure Heredity (2009) 103, 364–367; doi:10.1038/hdy.2009.86; the effect of the global rising of temperatures on the genetic published online 29 July 2009 Keywords: inversion polymorphism; global warming; thermal adaptation Drosophila subobscura is a Palaearctic species that has been probably originated from individuals from the other studied extensively by population and evolutionary (Ayala et al., 1989). geneticists for more than 70 years. In 1978 it was In the Palaearctic region, Prevosti (1974) and others discovered in Puerto Montt, Chile; within a few years it (reviewed in Krimbas and Loukas, 1980) determined that extended over much of Chile and into Argentina and the frequencies of many of the chromosome arrange- became the most common drosophilid in many places. In ments of D. subobscura vary in clinal patterns that 1982, it appeared in the American northwest, shortly are correlated with latitude. The association between thereafter it was found extensively distributed from climatic variables and the D. subobscura chromosomal southern British Columbia, through Washington and polymorphism has been interpreted as the result of Oregon, into central California. The karyotype of adaptation, although some authors have argued that D. subobscura consists of five acrocentric chromosomes, historical factors could explain the correlations without named A, J, U, E and O, plus a small dot–like invoking adaptive factors (Krimbas and Loukas, 1980). chromosome. Variations in sequence arrangement have The American populations, however, offer a rare been found in every one of the five large chromosomes: opportunity to test the role of selection in maintaining more than 80 different arrangements in total. There are the inversion-frequency clines: soon after the discovery differences between localities, but in every population of the species in America (3 years in the case of South most or all five chromosomes are polymorphic. The American populations), the frequencies of the chromo- frequencies of the various chromosomal arrangements some arrangements in nine South American and seven are remarkably similar in South America and in North North American populations were analysed (Prevosti America. The presence of the same 19 sequences, of 80 et al., 1988). Correlations between chromosomal arrange- known sequences, and in similar frequencies on both ment frequencies and latitude were calculated for these continents suggest that the two colonizations are not populations. Signs of these correlations are highly independent; the colonizers of one of the two continents coincident with those found in the Old World. The correlation coefficients are statistically significant for six chromosome arrangements in South America and for six Correspondence: Dr J Balanya`, Departament de Gene`tica, Facultat de in North America (Ayala et al., 1989). If we ignore the Biologia, Universitat de Barcelona, Av. Diagonal, 645. Annex planta 2, significance of individual correlations and consider only 08028 Barcelona, Spain. their sign, 12 out of 16 correlations have the same sign in E-mail: [email protected] all three continents. Not all these correlations are This paper is dedicated to A Prevosti on the occasion of his 90th anniversary. independent. If we exclude one per chromosome, 9 of Received 18 May 2009; accepted 26 May 2009; published online 12 correlations are of the same sign in all three 29 July 2009 continents. The probability of this coincidence being Chromosomal polymorphism in Drosophila subobscura J Balanya` et al 365 due to chance, as shown by a sign test, is Po0.001. Thus, arrangements of all chromosomes had changed signifi- the initial evolution of chromosomal polymorphism on a cantly during this period in a systematic way: an increase continental scale was remarkably rapid and consistent. in the frequency of those arrangements typical of Although the signs of correlations between frequency southern latitudes and a decrease for those more and latitude were similar on all three continents, the common in northern latitudes were observed in all New World clines were nonetheless much shallower populations. These changes could be due to climatic than those in the Old World. Would the New World factors that are correlated with latitude, making the clines become steeper over time and, thus, continue to chromosomal composition of this species more ‘equator- converge on the Old World ones? To evaluate this ial’ (Sole´ et al., 2002). The same authors extended the possibility, additional samples were collected in North analysis to three Atlantic and three Central European and South America. This effort has resulted in a genetic populations, obtaining similar results (Balanya` et al., time series that now spans approximately two decades 2004). The genetic distances of the new populations to an on both continents and offers insights into the strength average southern population of reference had decreased and consistency of selection along latitudinal gradients in comparison with those of the old populations. Again, (Balanya` et al., 2003). Large samples were collected at six these changes could be the result of climatic factors that sites in South America in 1986 and 1999 and at seven are correlated with latitude; in particular, the assumption sites in North America in 1992 and 1994. Of the 18 gene that global warming was responsible for all the changes arrangements found on all three continents over the observed appeared rather likely. entire census period, between 14 and 17 (depending on Given the evidence of shifts in chromosome-arrange- the particular census), form clines of the same sign on all ment frequency in Europe, might a similar change be three continents. It is interesting to note that the clines in taking place in the American colonizing populations, as South and North America had not become steeper over would be expected from global climate warming? Six time as expected, but remained distinctly shallower than South American and seven North American populations those in the Old World. In fact, none of the 18 gene were resampled in 1999 and 2004, respectively, and their arrangements on either continent showed a significant chromosomal polymorphism compared with those of the increase in slope. We speculate that the shallower slope corresponding first samples. A similar analysis that the may be due to the more limited number of inversions, one made in the Old World populations was then carried coupled with a general pattern of weak heterosis out. Table 1 shows the number of positive and negative (Mestres et al., 2001): all else being equal, more gene differences in each of the American subcontinents arrangements for a given chromosome allow more ways between the frequencies in the old and new samples to be a heterozygote. Coupled with graded selection for those arrangements showing significant positive or pressures along the cline plus some gene flow, the fewer negative correlation coefficients with latitude in Europe inversions would mean more shallow slopes. Indeed, the (Menozzi and Krimbas, 1992). These results show the slopes of the steepest clines (per each chromosome) in same trend as in the Old World: those arrangements the New World are suggestively correlated with the whose frequency shows a positive correlation coefficient number of gene arrangements (Pearson’s r ¼ 0.569, with latitude (potentially adapted to colder environ- t[8] ¼ 1.96, P ¼ 0.085) for that chromosome. ments) tend to be found at lower frequency in the new The adaptive value of the chromosomal polymorphism samples, whereas those with negative correlation coeffi- of D. subobscura and the capacity to respond very rapidly cient tend to increase their frequency. These long term and consistently to different environmental conditions changes detected in the chromosomal polymorphism of makes it a valuable tool to monitor global change. Newer D. subobscura in three discontinuous areas match those samples of inversion frequencies have been obtained for expected to take place in response to global warming. the colonizing populations since these first analyses:
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